1887

Abstract

A human mastadenovirus D (HAdV-D) isolated from diarrhoeal faeces of an allogeneic haematopoietic stem cell transplant (SCT) recipient was found to be non-typable by sequencing of loops 1 and 2 of the hexon main neutralization epitope (‘imputed serology’). In contrast to HAdV-C, HAdV-D infections are rarely observed in SCT patients. Therefore, the whole genome of this isolate was sequenced and phylogenetically analysed. In addition, microneutralization testing with type-specific antisera was performed. A complete genomic sequence of 35.2 kb in length with a GC content of 57  % was obtained and found to be distantly related to HAdV-D27 (96.25 % identity). Imputed serology implicated a new type with a nucleotide sequence identity of only 96.11 % to HAdV-D37 (loop 1) and 95.76 % to HAdV-D30 and HAdV-D37 (loop 2). Microneutralization testing confirmed that this clinical isolate was not neutralized by HAdV-D37- or HAdV-D30-specific antisera. The penton base gene showed a novel sequence, which clustered with HAdV-D38, but bootscan analysis indicated an intra-penton recombination event with HAdV-D60. Another recombination event was detected within the early gene region E3 with the 12.2 kDa and CR1-α genes derived from HAdV-D58. Moreover, the E4 region was derived from HAdV-D13, but all these genes had evolved significantly from their ancestors. By contrast, the recombinant fibre gene was almost 100 % identical to HAdV-D29. In conclusion, the genomics of this novel HAdV, designated the HAdV-D70 [P70H70F29] prototype, supported the significance of multiple recombinations in the phylogeny of HAdV-D.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.000196
2015-09-01
2024-04-20
Loading full text...

Full text loading...

/deliver/fulltext/jgv/96/9/2734.html?itemId=/content/journal/jgv/10.1099/vir.0.000196&mimeType=html&fmt=ahah

References

  1. Alissa Alkhalaf M., Al Qurashi Y.M., Guiver M., Cooper R.J. 2014; Genome sequences of three species D adenoviruses isolated from AIDS patients. Genome Announc 2:e01267–e01213 [View Article][PubMed]
    [Google Scholar]
  2. Brudno M., Do C.B., Cooper G.M., Kim M.F., Davydov E., Green E.D., Sidow A., Batzoglou S., NISC Comparative Sequencing Program. 2003; lagan and Multi-lagan: efficient tools for large-scale multiple alignment of genomic DNA. Genome Res 13:721–731 [View Article][PubMed]
    [Google Scholar]
  3. Crawford-Miksza L.K., Schnurr D.P. 1996; Adenovirus serotype evolution is driven by illegitimate recombination in the hypervariable regions of the hexon protein. Virology 224:357–367 [View Article][PubMed]
    [Google Scholar]
  4. de Jong J.C., Muzerie C.J., Wermenbol A.G., Wigand R., Keller D., Wadell G., Schaap G.J. 1981; Adenovirus 37: identification and characterization of a medically important new adenovirus type of subgroup D. J Med Virol 7:105–118 [View Article][PubMed]
    [Google Scholar]
  5. De Jong J.C., Wermenbol A.G., Verweij-Uijterwaal M.W., Slaterus K.W., Wertheim-Van Dillen P., Van Doornum G.J., Khoo S.H., Hierholzer J.C. 1999; Adenoviruses from human immunodeficiency virus-infected individuals, including two strains that represent new candidate serotypes Ad50 and Ad51 of species B1 and D, respectively. J Clin Microbiol 37:3940–3945[PubMed]
    [Google Scholar]
  6. Echavarría M. 2008; Adenoviruses in immunocompromised hosts. Clin Microbiol Rev 21:704–715 [View Article][PubMed]
    [Google Scholar]
  7. Ganzenmueller T., Buchholz S., Harste G., Dammann E., Trenschel R., Heim A. 2011; High lethality of human adenovirus disease in adult allogeneic stem cell transplant recipients with high adenoviral blood load. J Clin Virol 52:55–59 [View Article][PubMed]
    [Google Scholar]
  8. Garnett C.T., Erdman D., Xu W., Gooding L.R. 2002; Prevalence and quantitation of species C adenovirus DNA in human mucosal lymphocytes. J Virol 76:10608–10616 [View Article][PubMed]
    [Google Scholar]
  9. Garnett C.T., Talekar G., Mahr J.A., Huang W., Zhang Y., Ornelles D.A., Gooding L.R. 2009; Latent species C adenoviruses in human tonsil tissues. J Virol 83:2417–2428 [View Article][PubMed]
    [Google Scholar]
  10. Hage E., Huzly D., Ganzenmueller T., Beck R., Schulz T.F., Heim A. 2014; A human adenovirus species B subtype 21a associated with severe pneumonia. J Infect 69:490–499 [View Article][PubMed]
    [Google Scholar]
  11. Hierholzer J.C., Wigand R., Anderson L.J., Adrian T., Gold J.W. 1988; Adenoviruses from patients with AIDS: a plethora of serotypes and a description of five new serotypes of subgenus D (types 43-47). J Infect Dis 158:804–813 [View Article][PubMed]
    [Google Scholar]
  12. Hierholzer J.C., Stone Y.O., Broderson J.R. 1991; Antigenic relationships among the 47 human adenoviruses determined in reference horse antisera. Arch Virol 121:179–197 [View Article][PubMed]
    [Google Scholar]
  13. Ivanova O.E., Yurashko O.V., Eremeeva T.P., Baikova O.Y., Morozova N.S., Lukashev A.N. 2012; Adenovirus isolation rates in acute flaccid paralysis patients. J Med Virol 84:75–80 [View Article][PubMed]
    [Google Scholar]
  14. Jones M.S. II, Harrach B., Ganac R.D., Gozum M.M., Dela Cruz W.P., Riedel B., Pan C., Delwart E.L., Schnurr D.P. 2007; New adenovirus species found in a patient presenting with gastroenteritis. J Virol 81:5978–5984 [View Article][PubMed]
    [Google Scholar]
  15. Kajon A.E., Dickson L.M., Metzgar D., Houng H.S., Lee V., Tan B.H. 2010; Outbreak of febrile respiratory illness associated with adenovirus 11a infection in a Singapore military training cAMP. J Clin Microbiol 48:1438–1441 [View Article][PubMed]
    [Google Scholar]
  16. Kajon A.E., Lamson D., Shudt M., Oikonomopoulou Z., Fisher B., Klieger S., St George K., Hodinka R.L. 2014; Identification of a novel intertypic recombinant species D human adenovirus in a pediatric stem cell transplant recipient. J Clin Virol 61:496–502 [View Article][PubMed]
    [Google Scholar]
  17. Khoo S.H., Bailey A.S., de Jong J.C., Mandai B.K. 1995; Adenovirus infections in human immunodeficiency virus-positive patients: clinical features and molecular epidemiology. J Infect Dis 172:629–637 [View Article][PubMed]
    [Google Scholar]
  18. Lion T. 2014; Adenovirus infections in immunocompetent and immunocompromised patients. Clin Microbiol Rev 27:441–462 [View Article][PubMed]
    [Google Scholar]
  19. Lole K.S., Bollinger R.C., Paranjape R.S., Gadkari D., Kulkarni S.S., Novak N.G., Ingersoll R., Sheppard H.W., Ray S.C. 1999; Full-length human immunodeficiency virus type 1 genomes from subtype C-infected seroconverters in India, with evidence of intersubtype recombination. J Virol 73:152–160[PubMed]
    [Google Scholar]
  20. Lukashev A.N., Ivanova O.E., Eremeeva T.P., Iggo R.D. 2008; Evidence of frequent recombination among human adenoviruses. J Gen Virol 89:380–388 [View Article][PubMed]
    [Google Scholar]
  21. Madisch I., Harste G., Pommer H., Heim A. 2005; Phylogenetic analysis of the main neutralization and hemagglutination determinants of all human adenovirus prototypes as a basis for molecular classification and taxonomy. J Virol 79:15265–15276 [View Article][PubMed]
    [Google Scholar]
  22. Madisch I., Wölfel R., Harste G., Pommer H., Heim A. 2006; Molecular identification of adenovirus sequences: a rapid scheme for early typing of human adenoviruses in diagnostic samples of immunocompetent and immunodeficient patients. J Med Virol 78:1210–1217 [View Article][PubMed]
    [Google Scholar]
  23. Mynarek M., Ganzenmueller T., Mueller-Heine A., Mielke C., Gonnermann A., Beier R., Sauer M., Eiz-Vesper B., Kohstall U., other authors. 2014; Patient, virus, and treatment-related risk factors in pediatric adenovirus infection after stem cell transplantation: results of a routine monitoring program. Biol Blood Marrow Transplant 20:250–256 [View Article][PubMed]
    [Google Scholar]
  24. Nei M., Gojobori T. 1986; Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3:418–426[PubMed]
    [Google Scholar]
  25. Robinson C.M., Rajaiya J., Walsh M.P., Seto D., Dyer D.W., Jones M.S., Chodosh J. 2009; Computational analysis of human adenovirus type 22 provides evidence for recombination among species D human adenoviruses in the penton base gene. J Virol 83:8980–8985 [View Article][PubMed]
    [Google Scholar]
  26. Robinson C.M., Seto D., Jones M.S., Dyer D.W., Chodosh J. 2011a; Molecular evolution of human species D adenoviruses. Infect Genet Evol 11:1208–1217 [View Article][PubMed]
    [Google Scholar]
  27. Robinson C.M., Singh G., Henquell C., Walsh M.P., Peigue-Lafeuille H., Seto D., Jones M.S., Dyer D.W., Chodosh J. 2011b; Computational analysis and identification of an emergent human adenovirus pathogen implicated in a respiratory fatality. Virology 409:141–147 [View Article][PubMed]
    [Google Scholar]
  28. Robinson C.M., Singh G., Lee J.Y., Dehghan S., Rajaiya J., Liu E.B., Yousuf M.A., Betensky R.A., Jones M.S., other authors. 2013; Molecular evolution of human adenoviruses. Sci Rep 3:1812 [View Article][PubMed]
    [Google Scholar]
  29. Rosen L. 1960; A hemagglutination-inhibition technique for typing adenoviruses. Am J Hyg 71:120–128[PubMed]
    [Google Scholar]
  30. Ryan M.A., Gray G.C., Smith B., McKeehan J.A., Hawksworth A.W., Malasig M.D. 2002; Large epidemic of respiratory illness due to adenovirus types 7 and 3 in healthy young adults. Clin Infect Dis 34:577–582 [View Article][PubMed]
    [Google Scholar]
  31. Seto D., Chodosh J., Brister J.R., Jones M.S., Members of the Adenovirus Research Community. 2011; Using the whole-genome sequence to characterize and name human adenoviruses. J Virol 85:5701–5702 [View Article][PubMed]
    [Google Scholar]
  32. Singh G., Robinson C.M., Dehghan S., Jones M.S., Dyer D.W., Seto D., Chodosh J. 2013; Homologous recombination in E3 genes of human adenovirus species D. J Virol 87:12481–12488 [View Article][PubMed]
    [Google Scholar]
  33. Swenson P.D., Wadell G., Allard A., Hierholzer J.C. 2003; Adenoviruses. In Manual of Clinical Microbiology vol. 2 pp. 1404–1417 Edited by Murray P. R., Baron E. J., Pfaller M. A., Jorgensen J. H., Yolken R. A. Washington, DC: American Society for Microbiology;
    [Google Scholar]
  34. Veltrop-Duits L.A., van Vreeswijk T., Heemskerk B., Thijssen J.C., El Seady R., Jol-van der Zijde E.M., Claas E.C., Lankester A.C., van Tol M.J., Schilham M.W. 2011; High titers of pre-existing adenovirus serotype-specific neutralizing antibodies in the host predict viral reactivation after allogeneic stem cell transplantation in children. Clin Infect Dis 52:1405–1413 [View Article][PubMed]
    [Google Scholar]
  35. Walsh M.P., Chintakuntlawar A., Robinson C.M., Madisch I., Harrach B., Hudson N.R., Schnurr D., Heim A., Chodosh J., other authors. 2009; Evidence of molecular evolution driven by recombination events influencing tropism in a novel human adenovirus that causes epidemic keratoconjunctivitis. PLoS One 4:e5635 [View Article][PubMed]
    [Google Scholar]
  36. Wigand R. 1987; Pitfalls in the identification of adenoviruses. J Virol Methods 16:161–169 [View Article][PubMed]
    [Google Scholar]
  37. Yang Z., Zhu Z., Tang L., Wang L., Tan X., Yu P., Zhang Y., Tian X., Wang J., other authors. 2009; Genomic analyses of recombinant adenovirus type 11a in China. J Clin Microbiol 47:3082–3090 [View Article][PubMed]
    [Google Scholar]
  38. Zhang Z., Li J., Zhao X.Q., Wang J., Wong G.K., Yu J. 2006; KaKs_Calculator: calculating Ka and Ks through model selection and model averaging. Genomics Proteomics Bioinformatics 4:259–263 [View Article][PubMed]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/vir.0.000196
Loading
/content/journal/jgv/10.1099/vir.0.000196
Loading

Data & Media loading...

Supplements

Supplementary Data

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error